Relevance of the mouse model as a therapeutic approach for neutrophil proteinase 3-associated human diseases

International Immunopharmacology

Volumn 17, Issue 4, 2013, Pages 1198-1205

  Korkmaz, Brice ^a   Jenne, Dieter E ^b   Gauthier, Francis ^a  

^a Université Franaois Rabelais   (France)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

In vivo animal model; Neutrophil; Proteinase 3 (myeloblastin); Structure function

Indexed keywords

MYELOBLASTIN; NEUTROPHIL CYTOPLASMIC ANTIBODY;

ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; ANCA ASSOCIATED VASCULITIS; ANIMAL MODEL; BIOGENESIS; CELL DIFFERENTIATION; CELL SURFACE; CHROMOSOME 10; CHRONIC OBSTRUCTIVE LUNG DISEASE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; GLOMERULONEPHRITIS; HUMAN; IMMUNITY; LUNG DISEASE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PHYSICAL CHEMISTRY; PNEUMONIA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REVIEW; SYSTEMIC VASCULITIS; VASCULITIS; WEGENER GRANULOMATOSIS;

ABZ; ANCA; ANTINEUTROPHIL CYTOPLASM AUTO-ANTIBODIES; CATHEPSIN G; CG; CHRONIC OBSTRUCTIVE PULMONARY DISEASE; COPD; CYCLIN-DEPENDENT KINASE INHIBITOR-1; EDDNP; FLUORESCENCE RESONANCE ENERGY TRANSFER; FRET; GPA; GRANULOMATOSIS POLYANGIITIS; HNE; HPR3; HUMAN NEUTROPHIL ELASTASE; HUMAN PROTEINASE 3; IN VIVO ANIMAL MODEL; LIPOPOLYSACCHARIDE; LPS; MOUSE PROTEINASE 3; MPO; MPR3; MYELOPEROXIDASE; N-(2,4-DINITROPHENYL)ETHYLENEDIAMINE; NET; NEUTRAL SERINE PROTEINASES; NEUTROPHIL; NEUTROPHIL EXTRACELLULAR TRAPS; NSPS; ORTHO-AMINOBENZOIC ACID; P21; PROTEINASE 3 (MYELOBLASTIN); STRUCTURE FUNCTION; Α1-PROTEINASE INHIBITOR; ΑL-PI;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MICE; MYELOBLASTIN; NEUTROPHILS; PROTEIN CONFORMATION;

EID: 84890128446     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2013.07.003     Document Type: Review

References (108)

1. S. Dragonieri, O. Tongoussouva, A. Zanini, A. Imperatori, and A. Spanevello Markers of airway inflammation in pulmonary diseases assessed by induced sputum Monaldi Arch Chest Dis 71 2009 119 126
2. J.L. Simpson, R.J. Scott, M.J. Boyle, and P.G. Gibson Differential proteolytic enzyme activity in eosinophilic and neutrophilic asthma Am J Respir Crit Care Med 172 2005 559 565 (Pubitemid 41232966)
3. J.P. Lynch III, T.J. Standiford, M.W. Rolfe, S.L. Kunkel, and R.M. Strieter Neutrophilic alveolitis in idiopathic pulmonary fibrosis. The role of interleukin-8 Am Rev Respir Dis 145 1992 1433 1439
4. B. Korkmaz, M. Horwitz, D.E. Jenne, and A. Gauthier Neutrophil elastase, proteinase 3 and cathepsin G as therapeutic targets in human diseases Pharmacol Rev 62 2010
5. R.C. Kao, N.G. Wehner, K.M. Skubitz, B.H. Gray, and J.R. Hoidal Proteinase 3. A distinct human polymorphonuclear leukocyte proteinase that produces emphysema in hamsters J Clin Invest 82 1988 1963 1973 (Pubitemid 19054944)
6. C.T. Pham Neutrophil serine proteases: specific regulators of inflammation Nat Rev Immunol 6 2006 541 550 (Pubitemid 43980526)
7. C.T. Pham Neutrophil serine proteases fine-tune the inflammatory response Int J Biochem Cell Biol 40 2008 1317 1333
8. K. Kessenbrock, T. Dau, and D.E. Jenne Tailor-made inflammation: how neutrophil serine proteases modulate the inflammatory response J Mol Med (Berl) 89 2011 23 28
9. D. Garwicz, A. Lennartsson, S.E. Jacobsen, U. Gullberg, and A. Lindmark Biosynthetic profiles of neutrophil serine proteases in a human bone marrow-derived cellular myeloid differentiation model Haematologica 90 2005 38 44 (Pubitemid 40193752)
10. N.C. Perera, O. Schilling, H. Kittel, W. Back, E. Kremmer, and D.E. Jenne NSP4, an elastase-related protease in human neutrophils with arginine specificity Proc Natl Acad Sci U S A 109 2012 6229 6234
11. B. Korkmaz, T. Moreau, and F. Gauthier Neutrophil elastase, proteinase 3 and cathepsin G: physicochemical properties, activity and physiopathological functions Biochimie 90 2008 227 242 (Pubitemid 351187763)
12. E. Hajjar, T. Broemstrup, C. Kantari, V. Witko-Sarsat, and N. Reuter Structures of human proteinase 3 and neutrophil elastase - so similar yet so different FEBS J 277 2010 2238 2254
13. D.E. Jenne, J. Tschopp, J. Ludemann, B. Utecht, and W.L. Gross Wegener's autoantigen decoded Nature 346 1990 520 (Pubitemid 20238800)
14. R.J. Falk, W.L. Gross, L. Guillevin, G. Hoffman, D.R. Jayne, and J.C. Jennette Granulomatosis with polyangiitis (Wegener's): an alternative name for Wegener's granulomatosis J Am Soc Nephrol 22 2012 587 588
15. S.K. Frankel, and M.I. Schwarz The pulmonary vasculitides Am J Respir Crit Care Med 186 2012 216 224
16. R. Kettritz How anti-neutrophil cytoplasmic autoantibodies activate neutrophils Clin Exp Immunol 169 2012 220 228
17. N.J. Sinden, and R.A. Stockley Proteinase 3 activity in sputum from subjects with alpha-1-antitrypsin deficiency and COPD Eur Respir J 2012
18. W.C. Groutas, D. Dou, and K.R. Alliston Neutrophil elastase inhibitors Expert Opin Ther Pat 21 2011 339 354
19. M. Baggiolini, U. Bretz, B. Dewald, and M.E. Feigenson The polymorphonuclear leukocyte Agents Actions 8 1978 3 10 (Pubitemid 8274267)
20. G. Jégot, C. Derache, S. Castella, H. Lahouassa, E. Pitois, and M.L. Jourdan A substrate-based approach to convert SerpinB1 into a specific inhibitor of proteinase 3, the Wegener's granulomatosis autoantigen FASEB J 2011
21. C. Epinette, C. Croix, L. Jaquillard, S. Marchand-Adam, C. Kellenberger, and G. Lalmanach A selective reversible azapeptide inhibitor of human neutrophil proteinase 3 derived from a high affinity FRET substrate Biochem Pharmacol 83 2012 788 796
22. S.D. Shapiro, N.M. Goldstein, A.M. Houghton, D.K. Kobayashi, D. Kelley, and A. Belaaouaj Neutrophil elastase contributes to cigarette smoke-induced emphysema in mice Am J Pathol 163 2003 2329 2335 (Pubitemid 37466476)
23. G.G. Brusselle, K.R. Bracke, T. Maes, A.I. D'Hulst, K.B. Moerloose, and G.F. Joos Murine models of COPD Pulm Pharmacol Ther 19 2006 155 165
24. Y. Taooka, A. Maeda, K. Hiyama, S. Ishioka, and M. Yamakido Effects of neutrophil elastase inhibitor on bleomycin-induced pulmonary fibrosis in mice Am J Respir Crit Care Med 156 1997 260 265 (Pubitemid 27293199)
25. A.D. Salama, and M.A. Little Animal models of antineutrophil cytoplasm antibody-associated vasculitis Curr Opin Rheumatol 24 2012 1 7
26. M.M. van Timmeren, and P. Heeringa Pathogenesis of ANCA-associated vasculitis: recent insights from animal models Curr Opin Rheumatol 24 2012 8 14
27. J.C. Jennette, R.J. Falk, and A.H. Gasim Pathogenesis of antineutrophil cytoplasmic autoantibody vasculitis Curr Opin Nephrol Hypertens 20 2011 263 270
28. M. Relle, T. Thomaidis, P.R. Galle, and A. Schwarting Comparative aspects of murine proteinase 3 Rheumatol Int 31 2011 1105 1111
29. O. Wiesner, R.D. Litwiller, A.M. Hummel, M.A. Viss, C.J. McDonald, and D.E. Jenne Differences between human proteinase 3 and neutrophil elastase and their murine homologues are relevant for murine model experiments FEBS Lett 579 2005 5305 5312 (Pubitemid 41395148)
30. T. Kalupov, M. Brillard-Bourdet, S. Dade, H. Serrano, J. Wartelle, and N. Guyot Structural characterization of mouse neutrophil serine proteases and identification of their substrate specificities: relevance to mouse models of human inflammatory diseases J Biol Chem 2009
31. D.E. Jenne, L. Frohlich, A.M. Hummel, and U. Specks Cloning and functional expression of the murine homologue of proteinase 3: implications for the design of murine models of vasculitis FEBS Lett 408 1997 187 190 (Pubitemid 27226793)
32. R.M. Baron, A.J. Choi, C.A. Owen, and A.M. Choi Genetically manipulated mouse models of lung disease: potential and pitfalls Am J Physiol Lung Cell Mol Physiol 302 2012 L485 L497
33. M.A. Little, B. Al-Ani, S. Ren, H. Al-Nuaimi, M. Leite Jr., and C.E. Alpers Anti-proteinase 3 anti-neutrophil cytoplasm autoantibodies recapitulate systemic vasculitis in mice with a humanized immune system PLoS One 7 2012 e28626
34. A.M. Coughlan, S.J. Freeley, and M.G. Robson Humanised mice have functional human neutrophils J Immunol Methods 385 2012 96 104
35. V. Kumar, and A. Sharma Neutrophils: Cinderella of innate immune system Int Immunopharmacol 10 2010 1325 1334
36. N. Borregaard Neutrophils, from marrow to microbes Immunity 33 2010 657 670
37. B. Amulic, C. Cazalet, G.L. Hayes, K.D. Metzler, and A. Zychlinsky Neutrophil function: from mechanisms to disease Annu Rev Immunol 30 2012 459 489
38. A.W. Segal How neutrophils kill microbes Annu Rev Immunol 23 2005 197 223 (Pubitemid 40563169)
39. N. Borregaard, and J.B. Cowland Granules of the human neutrophilic polymorphonuclear leukocyte Blood 89 1997 3503 3521 (Pubitemid 27227073)
40. M.B. Hampton, A.J. Kettle, and C.C. Winterbourn Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing Blood 92 1998 3007 3017 (Pubitemid 28492304)
41. S.D. Kobayashi, J.M. Voyich, C. Burlak, and F.R. DeLeo Neutrophils in the innate immune response Arch Immunol Ther Exp (Warsz) 53 2005 505 517 (Pubitemid 43035779)
42. D. Turk, V. Janjic, I. Stern, M. Podobnik, D. Lamba, and S.W. Dahl Structure of human dipeptidyl peptidase I (cathepsin C): exclusion domain added to an endopeptidase framework creates the machine for activation of granular serine proteases EMBO J 20 2001 6570 6582 (Pubitemid 33134188)
43. M.J. McGuire, P.E. Lipsky, and D.L. Thiele Generation of active myeloid and lymphoid granule serine proteases requires processing by the granule thiol protease dipeptidyl peptidase I J Biol Chem 268 1993 2458 2467 (Pubitemid 23057866)
44. A.M. Adkison, S.Z. Raptis, D.G. Kelley, and C.T. Pham Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis J Clin Invest 109 2002 363 371 (Pubitemid 34141810)
45. V. Brinkmann, U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, and D.S. Weiss Neutrophil extracellular traps kill bacteria Science 303 2004 1532 1535 (Pubitemid 38314426)
46. V. Papayannopoulos, and A. Zychlinsky NETs: a new strategy for using old weapons Trends Immunol 30 2009 513 521
47. V. Brinkmann, and A. Zychlinsky Beneficial suicide: why neutrophils die to make NETs Nat Rev Microbiol 5 2007 577 582 (Pubitemid 47074113)
48. A.B. Sturrock, R. Espinosa III, J.R. Hoidal, and M.M. Le Beau Localization of the gene encoding proteinase-3 (the Wegener's granulomatosis autoantigen) to human chromosome band 19p13.3 Cytogenet Cell Genet 64 1993 33 34 (Pubitemid 23225901)
49. A. Belaaouaj, C. Moog-Lutz, J. Just, A. Houzel-Charavel, S.D. Shapiro, and Y. Cayre Genomic organization and chromosomal localization of mouse proteinase 3 (myeloblastin) Mamm Genome 10 1999 210 212 (Pubitemid 29390504)
50. D. Bories, M.C. Raynal, D.H. Solomon, Z. Darzynkiewicz, and Y.E. Cayre Down-regulation of a serine protease, myeloblastin, causes growth arrest and differentiation of promyelocytic leukemia cells Cell 59 1989 959 968 (Pubitemid 20024607)
51. Y. Monczak, M. Trudel, W.W. Lamph, and W.H. Miller Jr. Induction of apoptosis without differentiation by retinoic acid in PLB-985 cells requires the activation of both RAR and RXR Blood 90 1997 3345 3355 (Pubitemid 27473402)
52. M. Zimmer, R.L. Medcalf, T.M. Fink, C. Mattmann, P. Lichter, and D.E. Jenne Three human elastase-like genes coordinately expressed in the myelomonocyte lineage are organized as a single genetic locus on 19pter Proc Natl Acad Sci U S A 89 1992 8215 8219
53. A. Sturrock, K.F. Franklin, and J.R. Hoidal Human proteinase-3 expression is regulated by PU.1 in conjunction with a cytidine-rich element J Biol Chem 271 1996 32392 32402 (Pubitemid 26422282)
54. V. Witko-Sarsat, E.M. Cramer, C. Hieblot, J. Guichard, P. Nusbaum, and S. Lopez Presence of proteinase 3 in secretory vesicles: evidence of a novel, highly mobilizable intracellular pool distinct from azurophil granules Blood 94 1999 2487 2496 (Pubitemid 29467698)
55. S. von Vietinghoff, G. Tunnemann, C. Eulenberg, M. Wellner, M. Cristina Cardoso, and F.C. Luft NB1 mediates surface expression of the ANCA antigen proteinase 3 on human neutrophils Blood 109 2007 4487 4493 (Pubitemid 46743419)
56. H. Pfister, M. Ollert, L.F. Frohlich, L. Quintanilla-Martinez, T.V. Colby, and U. Specks Antineutrophil cytoplasmic autoantibodies against the murine homolog of proteinase 3 (Wegener autoantigen) are pathogenic in vivo Blood 104 2004 1411 1418 (Pubitemid 39166519)
57. M. Fujinaga, M.M. Chernaia, R. Halenbeck, K. Koths, and M.N. James The crystal structure of PR3, a neutrophil serine proteinase antigen of Wegener's granulomatosis antibodies J Mol Biol 261 1996 267 278 (Pubitemid 26275808)
58. E. Hajjar, B. Korkmaz, and N. Reuter Differences in the substrate binding sites of murine and human proteinase 3 and neutrophil elastase FEBS Lett 581 2007 5685 5690 (Pubitemid 350179780)
59. I. Schechter, and A. Berger On the size of the active site in proteases. I. Papain Biochem Biophys Res Commun 27 1967 157 162
60. B. Korkmaz, E. Hajjar, T. Kalupov, N. Reuter, M. Brillard-Bourdet, and T. Moreau Influence of charge distribution at the active site surface on the substrate specificity of human neutrophil protease 3 and elastase. A kinetic and molecular modeling analysis J Biol Chem 282 2007 1989 1997 (Pubitemid 47076700)
61. E. Hajjar, B. Korkmaz, F. Gauthier, B.O. Brandsdal, V. Witko-Sarsat, and N. Reuter Inspection of the binding sites of proteinase3 for the design of a highly specific substrate J Med Chem 49 2006 1248 1260 (Pubitemid 43271881)
62. C. Koehl, C.G. Knight, and J.G. Bieth Compared action of neutrophil proteinase 3 and elastase on model substrates. Favorable effect of S′-P′ interactions on proteinase 3 catalysts J Biol Chem 278 2003 12609 12612 (Pubitemid 36800019)
63. N.V. Rao, N.G. Wehner, B.C. Marshall, W.R. Gray, B.H. Gray, and J.R. Hoidal Characterization of proteinase-3 (PR-3), a neutrophil serine proteinase. Structural and functional properties J Biol Chem 266 1991 9540 9548 (Pubitemid 21906690)
64. O. Wiesner, K.A. Russell, A.S. Lee, D.E. Jenne, M. Trimarchi, and G. Gregorini Antineutrophil cytoplasmic antibodies reacting with human neutrophil elastase as a diagnostic marker for cocaine-induced midline destructive lesions but not autoimmune vasculitis Arthritis Rheum 50 2004 2954 2965 (Pubitemid 39209534)
65. Q.L. Ying, and S.R. Simon Kinetics of the inhibition of proteinase 3 by elafin Am J Respir Cell Mol Biol 24 2001 83 89 (Pubitemid 32097511)
66. V. Witko-Sarsat, N. Reuter, and L. Mouthon Interaction of proteinase 3 with its associated partners: implications in the pathogenesis of Wegener's granulomatosis Curr Opin Rheumatol 22 2010 1 7
67. B. Korkmaz, A. Kuhl, B. Bayat, S. Santoso, and D.E. Jenne A hydrophobic patch on proteinase 3, the target of autoantibodies in Wegener granulomatosis, mediates membrane binding via NB1 receptors J Biol Chem 283 2008 35976 35982
68. W.H. Goldmann, J.L. Niles, and M.A. Arnaout Interaction of purified human proteinase 3 (PR3) with reconstituted lipid bilayers Eur J Biochem 261 1999 155 162 (Pubitemid 29166080)
69. B. Korkmaz, J. Jaillet, M.L. Jourdan, A. Gauthier, F. Gauthier, and S. Attucci Catalytic activity and inhibition of Wegener antigen proteinase 3 on the cell surface of human polymorphonuclear neutrophils J Biol Chem 284 2009 19896 19902
70. A. Dementiev, J. Dobo, and P.G. Gettins Active site distortion is sufficient for proteinase inhibition by serpins: structure of the covalent complex of alpha1-proteinase inhibitor with porcine pancreatic elastase J Biol Chem 281 2006 3452 3457 (Pubitemid 43845960)
71. C.G. Kallenberg, P. Heeringa, and C.A. Stegeman Mechanisms of disease: pathogenesis and treatment of ANCA-associated vasculitides Nat Clin Pract Rheumatol 2 2006 661 670 (Pubitemid 44830855)
72. D.J. Davies, J.E. Moran, J.F. Niall, and G.B. Ryan Segmental necrotising glomerulonephritis with antineutrophil antibody: possible arbovirus aetiology? Br Med J (Clin Res Ed) 285 1982 606 (Pubitemid 12042688)
73. G.S. Hoffman, and U. Specks Antineutrophil cytoplasmic antibodies Arthritis Rheum 41 1998 1521 1537 (Pubitemid 28459910)
74. P. Yang Comparative evaluation of unfixed and fixed human neutrophils for determination of antineutrophil cytoplasmic antibodies by indirect immunofluorescence J Clin Pathol 50 1997 677 680 (Pubitemid 27396072)
75. E.W. Walton Giant-cell granuloma of the respiratory tract (Wegener's granulomatosis) Br Med J 2 1958 265 270
76. M.F. Cotch, G.S. Hoffman, D.E. Yerg, G.I. Kaufman, P. Targonski, and R.A. Kaslow The epidemiology of Wegener's granulomatosis. Estimates of the five-year period prevalence, annual mortality, and geographic disease distribution from population-based data sources Arthritis Rheum 39 1996 87 92 (Pubitemid 26036382)
77. C.G. Kallenberg Pathogenesis of PR3-ANCA associated vasculitis J Autoimmun 30 2008 29 36
78. D. Reumaux, P. Duthilleul, and D. Roos Pathogenesis of diseases associated with antineutrophil cytoplasm autoantibodies Hum Immunol 65 2004 1 12 (Pubitemid 38209929)
79. H. Tadema, P. Heeringa, and C.G. Kallenberg Bacterial infections in Wegener's granulomatosis: mechanisms potentially involved in autoimmune pathogenesis Curr Opin Rheumatol 23 2011 366 371
80. F. Callea, G. Gregorini, A. Sinico, G. Gonzales, M. Bossolasco, and G. Salvidio Alpha 1-Antitrypsin (AAT) deficiency and ANCA-positive systemic vasculitis: genetic and clinical implications Eur J Clin Invest 27 1997 696 702 (Pubitemid 27368302)
81. V.L. Esnault, A. Testa, M. Audrain, C. Roge, M. Hamidou, and J.H. Barrier Alpha 1-antitrypsin genetic polymorphism in ANCA-positive systemic vasculitis Kidney Int 43 1993 1329 1332 (Pubitemid 23161420)
82. M. Needham, and R.A. Stockley Alpha 1-antitrypsin deficiency. 3: Clinical manifestations and natural history Thorax 59 2004 441 445 (Pubitemid 38624753)
83. H. Morris, M.D. Morgan, A.M. Wood, S.W. Smith, U.I. Ekeowa, and K. Herrmann ANCA-associated vasculitis is linked to carriage of the Z allele of alpha(1) antitrypsin and its polymers Ann Rheum Dis 70 2011 1851 1856
84. Lyons PA, Rayner TF, Trivedi S, Holle JU, Watts RA, Jayne DR, et al. Genetically distinct subsets within ANCA-associated vasculitis. N Engl J Med 367:214-223.
85. S. Weidner, W. Neupert, M. Goppelt-Struebe, and H.D. Rupprecht Antineutrophil cytoplasmic antibodies induce human monocytes to produce oxygen radicals in vitro Arthritis Rheum 44 2001 1698 1706 (Pubitemid 32642233)
86. R.J. Falk, R.S. Terrell, L.A. Charles, and J.C. Jennette Anti-neutrophil cytoplasmic autoantibodies induce neutrophils to degranulate and produce oxygen radicals in vitro Proc Natl Acad Sci U S A 87 1990 4115 4119 (Pubitemid 20217992)
87. A. Schreiber, F.C. Luft, and R. Kettritz Membrane proteinase 3 expression and ANCA-induced neutrophil activation Kidney Int 65 2004 2172 2183 (Pubitemid 38670003)
88. K. Kessenbrock, M. Krumbholz, U. Schonermarck, W. Back, W.L. Gross, and Z. Werb Netting neutrophils in autoimmune small-vessel vasculitis Nat Med 15 2009 623 625
89. P. Bini, J.E. Gabay, A. Teitel, M. Melchior, J.L. Zhou, and K.B. Elkon Antineutrophil cytoplasmic autoantibodies in Wegener's granulomatosis recognize conformational epitope(s) on proteinase 3 J Immunol 149 1992 1409 1415
90. A.A. Rarok, Y.M. van der Geld, C.A. Stegeman, P.C. Limburg, and C.G. Kallenberg Diversity of PR3-ANCA epitope specificity in Wegener's granulomatosis. Analysis using the biosensor technology J Clin Immunol 23 2003 460 468 (Pubitemid 38177667)
91. Y.M. Van Der Geld, P.C. Limburg, and C.G. Kallenberg Characterization of monoclonal antibodies to proteinase 3 (PR3) as candidate tools for epitope mapping of human anti-PR3 autoantibodies Clin Exp Immunol 118 1999 487 496
92. A. Kuhl, B. Korkmaz, B. Utecht, A. Kniepert, U. Schonermarck, and U. Specks Mapping of conformational epitopes on human proteinase 3, the autoantigen of Wegener's granulomatosis J Immunol 185 2010 387 399
93. F. Silva, A.M. Hummel, D.E. Jenne, and U. Specks Discrimination and variable impact of ANCA binding to different surface epitopes on proteinase 3, the Wegener's autoantigen J Autoimmun 35 2010 299 308
94. C.P. Rooney, C. Taggart, R. Coakley, N.G. McElvaney, and S.J. O'Neill Anti-proteinase 3 antibody activation of neutrophils can be inhibited by alpha1-antitrypsin Am J Respir Cell Mol Biol 24 2001 747 754 (Pubitemid 32550598)
95. M.E. Griffith, J.U. Lovegrove, G. Gaskin, D.B. Whitehouse, and C.D. Pusey C-antineutrophil cytoplasmic antibody positivity in vasculitis patients is associated with the Z allele of alpha-1-antitrypsin, and P-antineutrophil cytoplasmic antibody positivity with the S allele Nephrol Dial Transplant 11 1996 438 443 (Pubitemid 26092781)
96. B. Korkmaz, C. Kellenberger, M.C. Viaud-Massuard, and F. Gauthier Selective inhibitors of human neutrophil proteinase 3 2013 Curr Pharm Des
97. B. Korkmaz, P. Poutrain, E. Hazouard, M. de Monte, S. Attucci, and F.L. Gauthier Competition between elastase and related proteases from human neutrophil for binding to alpha1-protease inhibitor Am J Respir Cell Mol Biol 32 2005 553 559 (Pubitemid 40770134)
98. M. Segelmark, A.N. Elzouki, J. Wieslander, and S. Eriksson The PiZ gene of alpha 1-antitrypsin as a determinant of outcome in PR3-ANCA-positive vasculitis Kidney Int 48 1995 844 850
99. A. Schreiber, C.T. Pham, Y. Hu, W. Schneider, F.C. Luft, and R. Kettritz Neutrophil serine proteases promote IL-1beta generation and injury in necrotizing crescentic glomerulonephritis J Am Soc Nephrol 23 2012 470 482
100. E. Remold-O'Donnell, J.C. Nixon, and R.M. Rose Elastase inhibitor. Characterization of the human elastase inhibitor molecule associated with monocytes, macrophages, and neutrophils J Exp Med 169 1989 1071 1086 (Pubitemid 19085841)
101. K. Beatty, J. Bieth, and J. Travis Kinetics of association of serine proteinases with native and oxidized alpha-1-proteinase inhibitor and alpha-1-antichymotrypsin J Biol Chem 255 1980 3931 3934
102. J. Mestas, and C.C. Hughes Of mice and not men: differences between mouse and human immunology J Immunol 172 2004 2731 2738 (Pubitemid 38263654)
103. A.M. Condliffe, K. Davidson, K.E. Anderson, C.D. Ellson, T. Crabbe, and K. Okkenhaug Sequential activation of class IB and class IA PI3K is important for the primed respiratory burst of human but not murine neutrophils Blood 106 2005 1432 1440 (Pubitemid 41129612)
104. Strowig T, Rongvaux A, Rathinam C, Takizawa H, Borsotti C, Philbrick W, et al. Transgenic expression of human signal regulatory protein alpha in Rag2-/-gamma(c)-/- mice improves engraftment of human hematopoietic cells in humanized mice. Proc Natl Acad Sci U S A 108:13218-13223.
105. Tanaka S, Saito Y, Kunisawa J, Kurashima Y, Wake T, Suzuki N, et al. Development of mature and functional human myeloid subsets in hematopoietic stem cell-engrafted NOD/SCID/IL2rgammaKO mice. J Immunol 188:6145-155.
106. K. Kessenbrock, L. Frohlich, M. Sixt, T. Lammermann, H. Pfister, and A. Bateman Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin J Clin Invest 118 2008 2438 2447 (Pubitemid 351949772)
107. C.S. Rogers, D.A. Stoltz, D.K. Meyerholz, L.S. Ostedgaard, T. Rokhlina, and P.J. Taft Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs Science 321 2008 1837 1841
108. D. Campanelli, M. Melchior, Y. Fu, M. Nakata, H. Shuman, and C. Nathan Cloning of cDNA for proteinase 3: a serine protease, antibiotic, and autoantigen from human neutrophils J Exp Med 172 1990 1709 1715